Abstract
Fermented tropical leaf meals (FTLM) are currently added to chicken feed to improve chicken productivity due to their reported nutritional and medicinal benefits. However, the effects of FTLM on broiler productivity and health are less clear. Thus, this meta-analysis was designed to assess the effects of FTLM on the performance outcomes of broilers Eleven controlled studies were retrieved and used to explore the impacts of dietary FTLM supplementation on growth performance [feed intake (FI), feed conversion ratio (FCR), average daily gain (ADG)], blood lipids, slaughter performance (abdominal fat, breast and thigh muscles weight), meat quality [pH, drip loss, shear force, lightness (L*), redness (a*), and yellowness (b*)], and intestinal histomorphology [villus height (VH), crypt depth (CD) and VH/CD values] of broilers. Subgroup and meta-regression analyses of the effects of moderators (i.e., leaf meal type, supplementation level, broiler strains, rearing phase, and fermentation microbes) on the growth performance of broilers were also assessed. Results show that dietary FTLM supplementation increased FI [standardised mean difference (SMD) = 0.11; 95% confidence interval (CI): 0.02, 0.20; P < 0.0001], improved ADG (SMD = 0.33; 95% CI: 0.23, 0.43; P < 0.0001) and FCR (SMD = − 0.21; 95% CI: − 0.30, − 0.11; P < 0.0001) in broilers. In addition, FTLM enhanced slaughter performance, meat quality, and intestinal histomorphology of broilers. Broilers fed 0—5 g/kg feed FTLM had better FI, FCR, and ADG than the controls taking significant heterogeneity into account. Meta-regression revealed that analysed moderators influenced growth performance results and accounted for some of the sources of heterogeneity. It can be concluded that up to 5 g/kg of FTLM can be added to broiler feed to improve growth performance, intestinal histomorphology, slaughter performance, and meat quality without adverse effects on dressing percentage and blood lipid profiles.
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Introduction
Due to the escalating cost of conventional feedstuffs, leaf meals from tropical plants are now added to poultry feed to reduce production costs and improve productivity and product quality (Manyelo et al. 2022; Niu et al. 2023). Tropical climate is endowed with a diversity of plants that can yield large leaf biomass throughout the year (Okoli et al. 2019). Leaf meals of tropical plants are high in essential nutrients (vitamins, crude proteins, and minerals), polysaccharides, and bioactive components such as polyphenols and flavonoids (Mat et al. 2020; Shi et al. 2021; Sugiharto 2021). Researchers have demonstrated that supplementation of high levels of tropical leaf meals (TLM) in the chicken diet results in poor performance and product quality (Modisaojang-Mojanaja et al. 2019; Ogbuewu and Mbajiorgu 2019; Manyelo et al. 2022). The reasons for the very poor performance of chickens fed higher levels of TLMs are not clear but may be ascribed to their high crude fibre content, imbalance amino acid profile, poor digestibility, and the presence of anti-physiological agents. It is therefore vital to explore ways of adding more values to TLMs for optimal results as is the case with other feed resources high in crude fibre (Chukwukaelo et al. 2018; Ahiwe et al. 2022).
Chemically, the bioactive components in tropical leaves are polyphenols, flavonoids, organic acids, and terpenoids (Cao et al. 2012; Niu et al. 2017), which contribute to their antimicrobial and antioxidative activities. Research has shown that flavonoids isolated from tropical plants have positive effects on lipid metabolism which may be related to their antioxidant properties (Feng et al. 2011; Cao et al. 2012; Arora and Itankar 2018). Studies have confirmed that TLMs have the following pharmacological activities: anti-inflammatory, antiplatelet, antiviral, anticancer, neuro-protection, and cardio-protection effects (Liu et al. 2013; Niu et al. 2017; Amodeo et al. 2019). The feeding value of TLMs is influenced by their low to moderate levels of anti-nutritional factors, such as trypsin inhibitors, pectin, phytate, saponins, tannins, and several others (Pachauri et al. 2017).
The use of fermentation as a method for increasing the digestibility of novel feed resources has been stated (Sugiharto and Ranjitkar 2019; Shi et al. 2021). Fermentation has been found to improve nutritional and functional values of TLMs as well as enhance performance parameters and product quality of broilers (Sugiharto and Ranjitkar 2019; Shi et al. 2021). Fermented TLM has also been reported to improve productivity of animals other than broilers (Zhou et al. 2015; Lee et al. 2019). However, there are variable results on the impacts of dietary fermented TLM on broiler productivity and meat quality (Cao et al. 2012; Mandey et al. 2015; Santoso et al. 2015, 2018; Kim et al. 2017; Manihuruk et al. 2018; Niu et al. 2019), and this discrepancy could be attributed to differences in broiler genetics, microorganisms implicated in the fermentation process, substrate used, composition of TLM, quantity of TLM incorporated into the diet and several other factors known to affect chicken performance (Ditengou et al. 2023; Ogbuewu and Mbajiorgu 2023). Thus, it is pertinent to systematically summarise the findings of published studies that investigated the effects of FTLM on broiler chicken performance and product quality to enhance the use of these large volumes of information in evidence-based decision-making process. This study, therefore aimed to evaluate the meta-analytic effect of FTLM supplementation on growth performance, blood lipids, intestinal histomorphology, slaughter performance, and meat quality of broilers.
Materials and methods
Search strategy and study selection process
PubMed, Scopus Google Scholar, and ScienceDirect databases were searched for articles on the topic using combinations of search terms and queries following the guideline for reporting systematic reviews and meta-analyses (Moher et al. 2009). Four hundred and sixty-nine (469) articles were identified via searches performed on the four databases of which eleven met the selection criteria (Fig. 1).
Data extraction and synthesis
Information on author name, publication year, study country, and moderators: broiler strains (Arbore Acres yellow feathered and Lohmann), leaf meal type (Ginkgo biloba, Morus alba, Sauropus androgynus and Chenopodium album), fermentation microbes (Lactobacillus spp, Bacillus subtilis, Aspergillus niger, Candida utilis, B. licheniform. Lactobacillus plantarum, Trichoderma harzianum, Neurospora crassa and Saccharomyces cerevisiae), supplementation level (0 – 14 g/kg feed), and rearing phase (starter, finisher and overall) was extracted from eligible studies (Table 1) and entered into a Microsoft Excel sheet. Supplementation level was further subdivided into 0—5, 6—10, and > 11—14 g/kg feed. The rearing phase comprised the starter phase (0—21 days), finisher phase (22–56 days), and overall phase (0–56 days). Extracted outcome data were FI, ADG, FCR, intestinal histomorphology (VH, CD and VH/CD ratio), blood lipids [cholesterol, triglycerides, high-density lipoprotein (HDL), and low-density lipoprotein (LDL)], slaughter performance (abdominal fat, breast, thigh, and dressing percentage), and meat quality parameters (pH, drip loss, shear force, L*, a*, and b*). Data were also extracted on the means and standard deviation (SD) or standard error (SE) for the control and experimental groups for each measured outcome. The extracted data was converted to a comma-separated value (CSV) file format which is the format accepted by OpenMEE software. Where a trial stated SE instead of SD, the SE was transformed to SD using the formula of Higgins and Deeks (2011): SD = SE × √n, where n is the number of broilers included in each treatment group.
Data analysis
Statistical analyses were executed in OpenMEE software designed and built by Wallace et al. (2016) at P < 0.05%. The execution flow chart of OpenMEE software has been described by Ogbuewu and Mbajiorgu (2020). Hedges’d commonly known as SMD was used to determine the pooled effect of FTLM on measured outcomes in broilers, and results were expressed at 95% confidence interval (CI). A random-effects model was used based on the assumption that the data being analysed are drawn from a hierarchy of different populations (Ogbuewu et al. 2022). Cochran’s Q-statistic and I2-test were used to assess and quantify statistical heterogeneity (Higgins et al. 2003). The meta-regression test was performed to determine the percentage of heterogeneity explained by analysed moderators. Publication bias was carried out to ascertain the validity of the results of the meta-analysis using Rosenberg’s fail-safe number (Rosenberg 2005). Pooled results were considered robust despite the evidence of publication bias if Nfs > 5 × n + 10, where, n = dataset (Jennions et al. 2013).
Results
Growth performance
The pooled mean FI as presented in Fig. 2 showed that broilers fed FTLM had higher values than the control. The subgroup analyses of the effect of moderators on FI are shown in Table 2. Arbor Acres strain offered FTLM supplementation had significantly higher FI than the Lohmann strain, but had similar FI with the Yellow feathered strain. Broilers fed FTLM at 0—5 g/kg feed recorded higher FI than the control. Leaf meal type had effect on FI, with broilers on fermented G. biloba leaf meal having significantly higher FI than those on fermented S. androgynus leaf meal. Starter broilers fed FTLM recorded higher FI than the control. In comparison to the controls, broilers fed TLM fermented with T. harzianum had significantly reduced FI while those fed diet containing fermented blends of A. niger and C. utilis had statistically increased FI. In contrast, broilers fed TLM fermented with A. niger, B. subtilis, B. licheniform, C. utilis, blends of Lactobacillus, Saccharomycetes, and B. subtilis, mixtures of B. subtilis, L. plantarum and S. cerevisiae had comparable FI with the control.
As displayed in Fig. 3, a significant difference occurred in FCR (SMD = − 0.21; 95% CI: − 0.30, − 0.11; P < 0.001) between broilers on treatment and control diets. Results of subgroup analyses of the impact of moderators on FCR are presented in Table 3. There was no effect of broiler strains on FCR between broilers in control and treatment groups; however, superior FCR was reported in Arbor Acres and Lohmann strains when compared with control. Broilers offered FTLM at 0 – 5 g/kg feed had better FCR than the control. Broilers fed fermented G. biloba leaf meal had better FCR (SMD = − 0.23; 95% CI: − 0.31, − 0.16) than those that received M. alba leaf meal (SMD = − 0.07; 95% CI: − 0.87, − 0.73) and S. androgynus leaf meal (SMD = 0.22; 95% CI: 0.03, 0.42). Also, broilers fed S. androgynus leaf meal had poor FCR (SMD = 0.22; 95% CI: 0.03, 0.42) compared to those offered M. alba leaf meal (SMD = − 0.07; 95% CI: − 0.87, − 0.73). Starter and finisher broilers fed FTLM recorded lower FCR than the control. Broilers fed TLM fermented with A. niger had better FCR than broilers offered TLM fermented with T. harzianum. Similarly, broilers fed TLM fermented with B. subtilis, B. licheniform, T. harzianum and blends of B. subtilis, L. plantarum, and S. cerevisiae had better FCR than the control.
The ADG as displayed in Fig. 4 suggests that broilers fed FTLM gained more weight than the control broilers. The restricted subgroup analyses of the effect of moderators on ADG as shown in Table 4 indicate that Arbor Acres and Yellow feathered broilers fed FTLM at 0 – 5 g/kg feed had heavier ADG than the Lohmann broiler strain. Similarly, broilers that received fermented leaf meals of G. biloba, M. alba, and C. album gained more weight than those that received fermented S. androgynus leaf meal. Broilers fed TLM fermented with a mixture of A. niger and C. utilis had superior ADG than those fed diet fermented with A. niger, T. harzianum, B. subtilis, B. licheniform, C. utilis, and blends of B. subtilis, L. plantarum, and S. cerevisiae.
Blood lipid profiles and intestinal histology
Data on blood lipids of broilers fed FTLM are shown in Table 5. Fermented TLM had a reduction effect on blood cholesterol content, although the effect was not significant (SMD = − 0.14; 95% CI: − 0.51, 0.24; P = 0.482). There was no treatment effect on triglyceride levels in broilers. However, the HDL value of broilers on dietary FTLM intervention was numerically higher than broilers on the control. Likewise, LDL value in broilers fed FTLM was numerically lower than those on the control diet. The effect of dietary FTLM intervention on intestinal histomorphology of broilers fed FTLM-based diets is shown in Table 6. Birds on dietary FTLM supplementation had significantly lower crypt depth (CD) and higher villi height (VH) and VH/CD of the duodenum than the control. There was treatment on the histoarchitecture of the jejunum and ileum with broilers fed FTLM having lower CD and VH/CD values than the control. In contrast, dietary FTLM supplementation had no effect on VH values of the jejunum and ileum in broilers.
Slaughter performance and meat quality
The slaughter performance of broilers fed FTLM-based diets is illustrated in Table 7. There was no significant difference in dressing percentage between broilers in the control and the treatment groups. In contrast, there was a treatment effect on thigh muscle weight (SMD = 0.50; 95% CI: 0.08, 0.92; P = 0.020) and breast muscle weight (SMD = 0.86; 95% CI: 0.48, 1.24; P < 0.001) between the groups. The abdominal fat weight was lower on the FTLM diet (SMD = − 0.63; 95% CI: − 0.90, − 0.35; P < 0.001) than the control. The influence of FTLM on the breast muscle quality of broilers is shown in Table 8. The breast muscle of broilers fed FTLM had significantly higher pH and reduced drip loss, shear force, and b* compared with the control. The breast muscle of broiler chickens offered FTLM had numerically higher L* and a* values than the control. There was a significant treatment effect on pH, drip loss, and shear force, with thigh muscles from broilers fed FTLM having significantly higher pH (SMD = 1.85; 95% CI: 0.96, 2.74; P < 0.001), and significantly lower drip loss (SMD = − 0.68; 95% CI: − 1.14, − 0.22; P = 0.004) and shear force (SMD = − 0.22; 95% CI: − 0.39, − 0.05; P = 0.010) when compared with the control (Table 9). The L* and b* values of thigh muscle were reduced by dietary FTLM. In contrast, there was no effect of FTLM on the a* value of broilers.
Moderator and publication bias analyses
Table 10 shows that supplementation levels is not a significant predictor of FI (P = 0.427; R2 = 0%), FCR (P = 0.076; R2 = 4%), and ADG (P = 0.249; R2 = 3%) in broilers. Likewise, rearing phase is not a significant predictor of FI (P = 0.124; R2 = 3%) and ADG (P = 0.096; R2 = 3%) in broilers. In contrast, there was a significant relationship between FI and aspects of analysed moderators. Results indicate that broiler strains (P = 0.001; R2 = 70%), LMT (P = 0.001; R2 = 72%), and fermentation microbes (P = 0.001; R2 = 74%) were significant predictors of ADG in broilers fed FTLM. Table 11 shows evidence of publication bias as the observed significance was lower than the target significance of 0.05 for FI, FCR, and ADG.
Discussion
The use of TLMs as feed resources in poultry production is on the increase due to their health and nutritional benefits (Sugiharto 2021; Shi et al. 2021). However, their large-scale use in broiler production is limited due to the fact the matured leaves are high in crude fibre and moderate in ANFs such as trypsin inhibitors, pectin, phytate, and tannins (Pachauri et al. 2017). Fermentation, particularly microbial fermentation, has received attention in recent times, due to its ability to reduce dietary crude fibre and anti-nutritional factors, increase nutritional and functional properties of leaf meals, and improve the growth performance of broilers (Missotten et al. 2013; Chukwukaelo et al. 2018; Yan et al. 2019). Tropical leaves are also rich sources of polysaccharides, unidentified growth factors, and flavonoids (Ndubuaku et al. 2014; Modisaojang-Mojanaja et al. 2019). Improved digestion and uptake of nutrients from the gastrointestinal tract of chickens may play a significant part in enhancing growth performance in chickens. The observed improvement in growth performance in broilers fed FTLM may be linked to a decrease in ANF levels in the diet, as well as the breakdown of complex biomass into small units by fermentation microorganisms, which is readily utilised by the birds (Shi et al. 2021; Sugiharto 2021). This finding is consistent with previous research that found superior FCR and increased ADG in chickens fed fermented herbal products (Shi et al. 2021; Sugiharto 2021). The increased ADG and FCR in broilers fed FTLM may be related to an improvement in intestinal health and function. The intestine is the principal site for immunity, nutrient digestion, and uptake in animals (Ogbuewu and Mbajiorgu 2022). The micro-anatomy of the intestine can give insight into intestinal health. Villus height, CD, and VH/CD value are the key parameters for assessing intestinal health and functions in poultry and livestock (Niu et al. 2019, 2022). To our knowledge, higher VH and VH/CD values and lower CD indicate a better ability of the intestine to absorb and utilise nutrients (Ogbuewu and Mbajiorgu 2022). The results of the present meta-analysis suggest that FTLM increased duodenum VH, duodenum, jejunum, and ileum VH/CD values and reduced duodenum, jejunum, and ileum CD values in broilers fed FTLM. These findings were in harmony with previous reports of others (Sugiharto 2021; Niu et al. 2022), which demonstrated improved absorptive capacity and functions of the small intestine of poultry offered fermented herbal products. In the current study, the increased growth performance of broilers offered FTLM is consistent with increased VH and VH/CD values and decreased CD. This implies that FTLM boosts broiler growth performance by increasing the absorptive capacity of the small intestine.
Blood biochemical indices reflect the function and metabolism of ingested feed in the animal body (Hu et al. 2015; Ogbuewu et al. 2015). There is a positive relationship between dietary intake and blood lipids in chickens (Ogbuewu et al. 2015). Low-density lipoprotein and HDL are the two major transport proteins for cholesterol in plasma. Earlier research has shown that flavonoids in fermented leaves can regulate lipid metabolism and reduce lipid accumulation (Wei et al. 2014), and this may explain the non-significant effect of FTLM on blood lipids of broilers. These results are consistent with the findings of Santoso et al. (2015), who found that fermented S. androgynus leaves did not affect blood lipids in broilers. In converse, Kamalia et al. (2014) stated that inclusion of unfermented herbal products in the chicken diet reduced the concentrations of blood cholesterol, triglyceride, and LDL, but elevated HDL content in broilers. The observed variation could be attributed to the fact that TLM used in the present meta-analysis was fermented.
Slaughter performance indicates the ability of animals to convert feed to muscle tissues. Muscle and visceral (abdominal) fat are the key indices to measure carcass yield and meat quality in broilers. In the current meta-analysis, the addition of FTLM to the broiler diets increased the weights of breast and thigh muscles. This finding is consistent with the results of Yang et al. (2008), who observed an increased in cut part (breast and thigh) weights of broilers fed fermented herbal products. This increase in cut-part weights was most likely due to the quality of FTLM-based diets leading to improvements in muscle protein accretion. Increased visceral fat deposition in broilers has a direct impact on processed meat products, lowering carcass yield, meat quality, and consumers’ purchase desire, as well as reducing economic benefits (Yu et al. 2019). Furthermore, increased abdominal fat deposition in broilers indicates poor dietary energy use efficiency. This study indicates that FTLM reduced abdominal fat yield in broilers, indicating the ability of bioactive compounds present in FTLM, especially flavonoids to regulate fat metabolism in broilers. Similarly, Ding et al. (2021) found reduced abdominal fat yield in broilers fed fermented herbal products. This finding suggests that the presence of probiotic organisms and functional bioactive compounds in FTLM might have influenced the lipid metabolic pathway, preventing fat deposition in the abdomen (Sugiharto 2021).
Muscle pH is one of the parameters affecting muscle characteristics post-slaughtering (Aberle et al. 2001). Furthermore, a rapid reduction in postmortem pH can result in protein denaturation that may lead to pale colour and poor water holding capacity (Cao et al. 2012). In the present study, FTLM improved the breast and thigh muscle pH values of broilers. This implies that FTLM can maintain the pH value of breast and thigh muscles in broilers. The pH obtained in this study was within the normal values of 5.70 and 5.96 reported by Fletcher et al. (2000) in broiler meat. Drip loss and cooking loss are markers used to determine the ability of muscles to retain water, i.e. water holding capacity (WHC). The significantly reduced drip loss in breast and thigh muscles of broilers offered FTLM compared to the controls, suggests an improvement in WHC of the meat. The improved drip loss suggests a reduction in the nutritional value via exudates that were released, and this resulted in firm and tender meat (Dabes 2001). Shear force (tenderness) is one of the important organoleptic parameters that determine consumer acceptability (Miller et al. 2001; Kannan et al. 2002). In this study, the results revealed that drip loss and shear force are consistent with that of pH values. The improvement in shear force may be related to enhanced antioxidative status, and flavonoids may play a beneficial role. Meat colour is a measure of quality and is vital due to its link with consumer acceptability (Pelicano et al. 2003). This study revealed that FTLM had similar breast muscle L* and a* values, but reduced the b* value. Broiler meat is also rich in polyunsaturated fatty acids making them susceptible to free radical attack (Arshad et al. 2011). Thus, the antioxidant status of muscles affects the meat quality. Dietary FTLM significantly reduced L*, a*, and b* values of thigh muscle. The likely cause of the significantly lower L ∗ value in broiler thigh muscle might be related to the increased antioxidant activity of FTLM, which protects muscle cells from oxidative damage and inhibits cell sap extravasation.
Moderator analysis and publication bias
This study revealed that broiler strains, LMT, and fermentation microbes were significant predictors of feed intake and accounted for about 16, 15, and 23% of variations in feed intake. Results also suggest that the Arbor Acres strain had a higher ability to utilise FTLM diets than the Lohmann strain, showing that Arbor Acres strain fed FTLM-supplemented diets was superior to the Lohmann strain in terms of feed intake, FCR, and ADG. These findings support the view that the genetics of chicken influence its production parameters (Sebola et al. 2015). Results show a small effect of LMT for feed intake, FCR and a large effect for ADG. This suggests that LMT is a significant predictor of ADG in broilers and accounted for most of the sources of heterogeneity. The significantly higher feed intake in broilers fed fermented G. biloba leaf meal compared with those fed fermented S. androgynus leaf meal, indicates the quality of the fermented G. biloba leaf meal.
The improved growth performance of broilers fed fermented TLM at 0 – 5 g/kg feed compared to control agrees with the earlier reports of Ding et al. (2021), who found sub-optimal performance of broilers offered high doses of FTLM due to the dilution of basic nutrients in the diet. This finding is consistent with the reports of Niu et al. (2019) who reported decreased FI and ADG in broilers fed high doses of fermented G. biloba leaf meal. Results also demonstrated that fermentation microbes is a limiting factor in this study and can lead to variable results in FI, FCR, and ADG among trials included in the meta-analysis. The significantly higher feed intake recorded in broilers fed TLM fermented with a mixture of A. niger and C. utilis when compared to those fed TLM individually fermented A. niger and T. harzianum indicate the high ability of these microbes to improve the quality of TLM during fermentation. There is little effect for rearing phase as a moderator for FCR. The percentage of heterogeneity not accounted for by the analysed moderators could be to the following factors: seasonal variations, storage conditions of the leaves, and stocking density not analysed in the meta-analysis. There is evidence of publication bias for FI, ADG, and FCR. The Rosenberg Nfs for the database was about 3, 5, and 15 folds higher than the thresholds needed to consider the mean effect size for FI, FCR, and ADG valid. As a result, publication bias was not an issue in this study because a large number of unpublished studies would be needed to alter the statistically significant effects of FTLM on FI, FCR, and ADG in broilers.
Conclusion
The results of this investigation demonstrated the potential of dietary FTLM supplementation to improve growth performance, intestinal histomorphology, slaughter performance, and meat quality of broilers without negative consequences on dressing percentage and blood lipid profiles. Restricted subgroup analysis results indicate that supplementation of FTLM at 0—5 g/kg feed is associated with significant improvement in growth performance parameters of broilers. However, future research should focus on determining the actual supplementation levels of FTLM that optimised all the production parameters of broilers. Meta-regression showed that analysed moderator variables were significant predictors of treatment effect and accounted for some of the sources of heterogeneity. The findings of the meta-analysis will help poultry farmers, animal nutritionists, and policy-makers to make an informed decision on the potential of FTLM to improve broiler productivity and meat quality.
Data availability
Data will be made available on reasonable request.
References
Aberle, E.D., Forrest, J.C., Gerrard, D.E. and Mills, E.W. (2001). Principles of Meat Science. 4th ed. Kendall/Hunt Publishing Co., IA.
Ahiwe, E.U., Ejiofor, I., Oladipupo, O.A., Ogbuewu, I.P., Aladi, N.O., Obikaonu, H.O. and Emenalom, O.O. (2022). Effect of composite enzyme supplementation on production parameters, intestinal segment measurements, and apparent nutrient digestibility of broiler chickens fed low energy and protein diets. Tropical Animal Health and Production, 54:399.
Amodeo, V., Marrelli, M., Pontieri, V., Cassano, R., Trombino, S., Conforti, F. and Statti, G. (2019). Chenopodium album L. and Sisymbrium officinale (L.) Scop.: phytochemical content and in vitro antioxidant and anti-inflammatory potential. Plants, 8:505.
Arora, S. and Itankar, P. (2018). Extraction, isolation and identification of flavonoid from Chenopodium album aerial parts. Journal of Traditional Complementary Medicine, 8:476–482.
Arshad, M. S., Anjum, F.M., Asghar, A., Khan, M.I., Yasin, M., Shahid, M. and EI-Ghorab, A.H. (2011). Lipid stability and antioxidant profile of microsomal fraction of broiler meat enriched with α-lipoic acid and α-tocopherol acetate. Journal of Agriculture and Food Chemistry, 59:7346–7352.
Cao, F.L., Zhang, X.H., Yu, W.W., Zhao, L.G. and Wang, T. (2012). Effect of feeding fermented Ginkgo biloba leaves on growth performance, meat quality, and lipid metabolism in broilers. Poultry Science, 91: 1210-1221.
Chukwukaelo, A.K., Aladi, N.O., Okeudo, N.J., Obikaonu, H.O., Ogbuewu, I.P. and Okoli, I.C. (2018). Performance and meat quality characteristics of broilers fed fermented mixtures of grated cassava roots and palm kernel cake as replacement for maize. Tropical Animal Health and Production, 50: 485-493.
Dabes, A. C. (2001). Properties of fresh meat. Revista nacional da carne, 25:32–40.
Ding, Y., Jiang, X., Yao, X., Zhang, H., Song, Z., He, X. and Cao, R. (2021). Effects of feeding fermented mulberry leaf powder on growth performance, slaughter performance, and meat quality in chicken broilers. Animals, 11: 3294.
Ditengou, J.I.C.P., Cho, S., Ahn, S., Chae, B., Jeon, E. and Choi, N. (2023). Effects of different triticale inclusion levels on broilers’ growth parameters: A meta-analysis. Veterinary and Animal Science, 23:100328.
Feng, L.J., Yu, C.H., Ying, K.J., Hua, J. and Dai, X.Y. (2011). Hypolipidemic and antioxidant effects of total flavonoids of Perilla frutescens leaves in hyperlipidemia rats induced by high-fat diet. Food Research International, 44:404–409.
Fletcher, D.L., Giao, M. and Smith, D.P. (2000). The relationship of raw broiler breast meat color and pH to cooked meat colour and pH. Poultry Science, 79:784-788.
Higgins, J.P., Thompson, S.G., Deeks, J.J. and Altman, D.G. (2003) Measuring inconsistency in meta-analyses. BMJ 327:557.
Higgins, J.P.T. and Deeks, J.J. (2011). Chapter 7: Selecting studies and collecting data. In: Higgins, J.P., Green, S., (Eds), Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 (updated March 2011). The Cochrane Collaboration, 2011. Available from http://handbook.cochrane.org/. (Accessed: 19th September, 2023).
Hu, Y.N., Wang, Y.W., Li, A.K., Wang, Z.S., Zhang, X.L., Yun, T.T., Qiu, L.W. and Yin, Y.H. (2015). Effects of fermented rapeseed meal on antioxidant functions, serum biochemical parameters and intestinal morphology in broilers. Food and Agricultural Immunology, 27: 1–12.
Jennions, M.D., Lortie, C.J., Rosenberg, M.S. and Rothstein, H.R. (2013). Chapter 14: Publication and related bias. In: Koricheva, J., Gurevitch, J., Mengersen, K. (Eds.), Handbook of Meta-Analysis in Ecology and Evolution. Princeton University Press, Princeton and London, pp. 207–236.
Kamalia, A., Mujenisa, K. and Natsir, A. (2014). Effect of adding various levels of katuk (Sauropus androgynus) leaf flour on cholesterol, triglycerides, LDL and HDL in broiler blood. Nutrition and Forage Bulletin 10: 12-18.
Kannan, G., Chawan, C.B., Kouakou, B. and Gelaye, S. (2002). Influence of packaging method and storage time on shear value and mechanical strength of intramuscular connective tissue of chevon. Journal of Animal Science, 80:2383–2389.
Kim, Y.J., Rubayet Bostami, A.B.M., Islam, M.M., Mun, H.S., Ko, S.Y. and Yang, C.J. (2017). Performance, immunity, meat composition and fatty acid pattern in broilers after dietary supplementation of fermented Ginkgo biloba and Citrus junos. Journal of Nutrition and Food Sciences, 7: 591.
Lee, A.R., Niu, K.M., Lee, W.D., Kothari, D. and Kim, S.K. (2019). Comparison of the dietary supplementation of Lactobacillus plantarum, and fermented and non-fermented Artemisia annua on the performance, egg quality, serum cholesterol, and egg yolk-oxidative stability during storage in laying hens. Brazilian Journal of Poultry Science, 21:001–008.
Liu, A.H., Bao, Y.M., Wang, X.Y., and Zhang, Z.X. (2013). CardioProtection by Ginkgo biloba extract in rats with acute myocardial infarction is related to Na+-Ca2+ exchanger. The American Journal Chinese Medicine, 41:789–800.
Mandey, J.S., Leke, J.R., Kaunang, W.B. and Kowel, Y.H.S. (2015). Carcass yield of broiler chickens fed banana (Musa paradisiaca) leaves fermented with Trichoderma viride. Journal of the Indonesian Tropical Animal Agriculture, 40: 229-233.
Manihuruk, F.H., Ismail, I., Rastina, R., Razali, R., Sabri, M., Zuhrawati, Z., Muhammad, M. and Jalaluddin, J. (2018). Effect of fermented Moringa (Moringa oleifera) leaf powder in feed to increase broiler carcass weight. Jurnal Medika Veterinaria, 12: 103-109.
Manyelo, T.G., Amenda Sebola, N.A. and Mabelebele, M. (2022). Effect of amaranth leaf meal on performance, meat, and bone characteristics of Ross 308 broiler chickens. PLoS ONE, 17(8): e0271903.
Mat, K., Taufik, H.A., Rusli, N.D., Hasnita, C.H., Al-Amsyar, S.M., Rahman, M.M. and Mohd, M. (2020). Effects of fermentation on the nutritional composition, mineral content and physical characteristics of banana leaves. IOP Conf. Series: Earth and Environmental Science, 596: 012089.
Miller, M.F., Carr, M.F., Ramsey, C.B., Crockett, K.L. and Hoover, L.C. (2001). Consumer thresholds for establishing the value of beef tenderness. Journal of Animal Science, 79:3062–3068.
Missotten, J.A., Michiels, J., Dierick, N., Ovyn, A., Akbarian, A. and De Smet, S. (2013). Effect of fermented moist feed on performance, gut bacteria and gut histomorphology in broilers. British Poultry Science, 54: 627–634.
Modisaojang-Mojanaja, M.M.C., Ogbuewu, I.P., Mokolopi, B.G., Oguttu, J.W. and Mbajiorgu, C.A. (2019). Mineral composition of Moringa oleifera leaf meal (MOLM) and the response of ross 308 broilers to MOLM supplementation. Applied Ecology and Environmental Research, 17: 8139 – 8150.
Moher, D., Liberati, A., Tetzlaff, J. and Altman, D.G. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Journal of Clinical Epidemiology, 62: 1006 - 1012.
Ndubuaku, U.M., Nwankwo, V.U. and Baiyeri, K.P. (2014). Influence of poultry manure application on the leaf amino acid profile, growth and yield of moringa (Moringa oleifera Lam.) plants. International Journal of Current Trends in Research, 2:390-396.
Niu, Y., Wan, X.L., Zhang, X.H., Zhao, L.G., He, J.T., Zhang, J.F., Zhang, L.L. and Wang, T. (2017). Effect of supplemental fermented Ginkgo biloba leaves at different levels on growth performance, meat quality, and antioxidant status of breast and thigh muscles in broiler chickens. Poultry Science, 96:869–877.
Niu, Y., Zhang, J.F., Wan, X.L., Huang, Q., He, J.T., Zhang, X.H., Zhao, L.G., Zhang, L.L. and Wang, T. (2019). Effect of fermented Ginkgo biloba leaves on nutrient utilisation, intestinal digestive function and antioxidant capacity in broilers. British Poultry Science, 60: 47-55.
Niu, K.M., Khosravic, S., Wang, Y., Zhai, Z., Wang, R., Liu, J., Cai, L., Li, J., Deng, L. and Wu, X. (2022). Multiomics-based functional characterization of hybrid fermented Broussonetia papyrifera: a preliminary study on gut health of laying hens. Fermentation, 8:547.
Niu, K, Wang, Y.F., Liang, X., Zhai, Z., Liu, J., Wang, R., Chen, G. and Wu, X. (2023). Impact of fermented Broussonetia papyrifera on laying performance, egg quality, lipid metabolism, and follicular development of laying hens. Poultry Science, 102:102569.
Ogbuewu, I.P. and Mbajiorgu, C.A. (2019). Potential of leaf and seed meals of tropical plants in chicken diet: effect on spermatozoa and egg production. Tropical Animal Health and Production, 51: 267-277.
Ogbuewu, I.P. and Mbajiorgu, C.A. (2020). Meta-analysis of the effect of ginger (Zingiber officinale) on health status, production indices and semen quality in chickens. Agricultural Research, 9:640–651.
Ogbuewu, I.P. and Mbajiorgu, C.A. (2022). Meta-analysis of responses of broiler chickens to probiotic-bacillus supplementation: Intestinal histomorphometry and serum immunoglobulin. Open Agriculture, 7:465-477.
Ogbuewu, I.P. and Mbajiorgu, C.A. (2023). Lipid profiles and production performance responses of laying hens to dietary Moringa oleifera leaf meal: systematic review and meta-analysis. Tropical Animal Health and Production, 55:277.
Ogbuewu, I.P., Emenalom, O.O. and Okoli, I.C. (2015). Alternative feedstuffs and their effects on blood chemistry and haematology of rabbits and chickens: a review. Comparative Clinical Pathology, 26: 277 – 286.
Ogbuewu, I.P., Mokolopi, B.G. and Mbajiorgu, C.A. (2022). Meta-analysis of growth performance indices of broiler chickens in response to turmeric (Curcuma longa L.) supplementation. Animal Feed Science and Technology, 283:115155.
Okoli, I.C., Udedibie, C.O.I., Achonwa, C.C., Ogbuewu, I.P., Anyanwu, N.J. and Enemor, V.H.A. (2019). Physicochemical characterizations of leaf meals derived from tropical plants as possible nutraceuticals in animal production. Asian Journal of Biological Sciences, 12: 693-701
Pachauri, T., Lakhani, A. and Kumari, K.M. (2017). Nutritional and anti-nutritional characterization of Chenopodium album seeds: a neglected wild species. International Journal of Nutrition and Agricultural Research, 4:9–21.
Pelicano, E.R.L., De Souza, P.A., De Souza, H.B.A., Oba, A., Norkus, E.A., Kodawara, L.M. and De Lima, T.M. (2003). Effect of different probiotics on broiler carcass and meat quality. Revista Brasileira de Ciencia Avicola, 5:207–214
Rosenberg, M.S. (2005). The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution, 59:464-468.
Santoso, U., Fenita, Y. and Kususiyah, K. (2015). Effect of fermented Sauropus androgynus leaves on blood lipid fraction and haematological profile in broiler chickens. Journal of the Indonesian Tropical Animal Agriculture, 40: 199-207.
Santoso, U., Fenita, Y. and Kususiyah, K. (2018). The Effect of fermented Sauropus androgynus plus bay leaf inclusion on the hematologic and lipid profiles of female broiler chickens. International Journal of Poultry Science, 17: 410-417.
Sebola, N.A., Mlambo, V., Mokoboki, H.K. and Muchenje, V. (2015). Growth performance and carcass characteristics of three chicken strains in response to incremental levels of dietary Moringa oleifera leaf meal. Livestock Science, 178: 202-208.
Shi, H., Yang, E., Li, Y., Chen, X. and Zhang, J. (2021). Effect of solid-state fermentation on nutritional quality of leaf flour of the drumstick tree (Moringa oleifera Lam.). Frontiers in Bioengineering and Biotechnology, 9:626628.
Sugiharto, S. (2021). Fermented leaves in broiler rations: effects on growth performance, physiological condition, and meat characteristics. Acta Veterinaria Eurasia, 47: 44-50.
Sugiharto, S. and Ranjitkar, S. (2019). Recent advances in fermented feeds towards improved broiler chicken performance, gastrointestinal tract microecology and immune responses: A review. Animal Nutrition, 5:1-10.
Syahruddin, E., Herawaty, R. and Ningrat, R.W.S. (2013). Effect of fermented Katuk leaf (Sauropus androgynus L. Merr.) in diets on cholesterol content of broiler chicken carcass. Pakistan Journal of Nutrition, 12: 1013-1018.
Wallace, B.C., Lajeunesse, M.J., Dietz, G., Dahabreh, I.J., Trikalinos, T.A., Schmid, C.H. and Gurevitch, J. (2016). OpenMEE: intuitive, opensource software for meta-analysis in ecology and evolutionary biology. Methods Ecology and Evolution, 8:941–947
Wei, T., Xiong, F.F., Wang, S.D., Wang, K., Zhang, Y.Y. and Zhang, Q.H. (2014). Flavonoid ingredients of Ginkgo biloba leaf extract regulate lipid metabolism through Sp1- mediated carnitine palmitoyltranferase 1A up-regulation. Journal of Biomedical Science, 21, 1–11.
Xie, M., Wang, R., Wang, Y., Liu, N. and Qi, J. (2021). Effects of dietary supplementation with fermented Chenopodium album L. on growth, nutrient digestibility, immunity, carcass characteristics and meat quality of broilers, Italian Journal of Animal Science, 20: 2063-2074.
Yan, J., Zhou, B., Xi, Y., Huan, H., Li, M., Yu, J., Zhu, H., Dai, Z., Ying, S., Zhou, W. et al. (2019). Fermented feed regulates growth performance and the cecal microbiota community in geese. Poultry Science, 98: 4673–4684.
Yang, X.Y., Li, Y.X. and Li, Y. (2008). Effect of Ginkgo biloba extract on growth performance, slaughter performance and immune index in broilers. Journal of Fujian Agriculture and Forestry University (Natural Science Edition in Chinese). 3:295–298.
Yu, W., Zhang, X., Ahmad, H., Zhao, L., Wang, T. and Cao, F. (2015). Intestinal absorption function of broiler chicks supplemented with ginkgo leaves fermented with Bacillus species. Pakistan Journal of Zoology, 47: 479-490.
Yu, L., Peng, Z., Dong, L., Wang, H. and Shi, S. (2019). Enterococcus faecium NCIMB 10415 supplementation improves the meat quality and antioxidant capacity of muscle of broilers. Journal of Animal Physiology and Animal Nutrition, 103: 1099–1106.
Zhang, X., Cao, F., Sun, Z., Yu, W., Zhao, L., Wang, G. and Wang, T. (2012). Effect of feeding Aspergillus niger-fermented Ginkgo biloba-leaves on growth, small intestinal structure and function of broiler chicks. Livestock Science, 147: 170–180
Zhang, X., Sun, Z., Cao, F., Ahmad, H., Yang, X., L. Zhao L. and Wang, T. (2015). Effects of dietary supplementation with fermented Ginkgo leaves on antioxidant capacity, intestinal morphology and microbial ecology in broiler chicks. British Poultry Science, 56:370-80.
Zhang, X., Sun, Z., Cai, J., Wang, G., Zhu, Z., Zhao, L. and Cao, F. (2020). Dietary supplementation with fermented radix astragalus-ginkgo leaves improves antioxidant capacity and meat quality in broilers. Pakistan Journal of Zoology, 52: 1571-1585.
Zhou, H., Wang, C., Ye, J., Chen, H. and Tao, R. (2015). Effects of dietary supplementation of fermented Ginkgo biloba L. residues on growth performance, nutrient digestibility, serum biochemical parameters and immune function in weaned piglets. Animal Science Journal, 86: 790-799.
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IPO, MM and CAM conceptualised and designed the study. Data collection and synthesis were carried by the IPO and MM. The first draft of the manuscript was written by IPO and CAM. MM edited the draft and all the authors read and approved the final manuscript.
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Ogbuewu, I.P., Mabelebele, M. & Mbajiorgu, C.A. Determination of performance response of broilers to fermented tropical leaf meal supplementation using meta-analytical method. Trop Anim Health Prod 56, 98 (2024). https://doi.org/10.1007/s11250-024-03944-w
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DOI: https://doi.org/10.1007/s11250-024-03944-w